Paulinella: An Emerging Model in Photosynthesis Research and Plastid Evolution

Origin of Primary Plastids Via Endosymbiosis

Paulinella chromatophoraThe origin of primary plastid (e.g., chloroplasts) is most likely traced back to a single primary endosymbiosis whereby a non−photosynthetic protist engulfed and enslaved photosynthetic cyanobacteria as cytoplasmic organelles. Descendants of these primitive photosynthetic eukaryotes likely gave rise to the red, green (including land plants), and glaucophyte algae, or collectively, the Plantae. By subsequent eukaryote−eukaryote (secondary and tertiary endosymbioses), plastids and photosynthesis spread into other eukaryotic groups (e.g., brown seaweeds, diatoms, and dinoflagellates) and gave rise to the astonishing biological diversity of photoautotrophic eukaryotes that govern food webs in the biosphere. Despite its importance to eukaryote evolution and the considerable amount of knowledge we have about plastid evolution, the understanding of primary plastid origins is limited because it occurred during the Proterozoic circa 1.5 billion years ago.

Our understanding of this pivotal event in the Earth’s history has recently been provided a fresh perspective with molecular studies of the green thecate amoeba Paulinella chromatophora, which was described by Robert Lauterborn more than a century ago. This little−known filose amoeba is a member of the presumed supergroup "Rhizaria" and is noteworthy because it contains two cyanobacterial−derived organelles termed chromatophores. Two key reasons why the chromatophores of Paulinella chromatophora are considered bona fide organelles (=plastids) rather than temporary endosymbionts are the apparent regulation of organelle division by the amoeba and the reduction by 2/3 (i.e., from ca. 3 Mb in free−living Prochlorococcus/Synechococcus cyanobacteria to circa 1.0 Mb in the Paulinella chromatophora) of the chromatophore gene coding potential through outright gene loss or gene transfer (endosymbiotic gene transfer, EGT) to the Paulinella chromatophora nuclear genome.

Why Sequence the Paulinella Genome?

Our current knowledge of eukaryote diversity identifies Paulinella chromatophora as a recent (circa 60 million years old) and fleetingly rare case of recruitment of cyanobacterial prey as permanent photosynthetic organelles, and unquestionably independent of the anciently evolved Plantae primary plastid. Several Paulinella chromatophora characteristics resemble the hypothetical early stages envisaged for the origin of the Plantae, making this photosynthetic amoeba an outstanding model for investigating organelle evolution and understanding the cellular, genomic, and molecular general process that gave rise to the Plantae ancestor.

Besides the photoautotrophic Paulinella chromatophora, three heterotrophic Paulinella species (i.e., Paulinella ovalis, Paulinella intermedia and Paulinella indentata) have been reported, but the phylogenetic relationships between the four Paulinella species are unknown. However, the ability of Paulinella ovalis to capture cyanobacterial prey makes it a reasonable assumption that the primary endosymbiosis occurred in the Paulinella chromatophora ancestor after its split from a heterotrophic branch of the Paulinellidae. In summary, we believe, that genomic investigations of the Paulinellidae lineage constitutes an extraordinary model for understanding organellogenesis.

Our project has its the main aims to determine draft nuclear genome sequences from the photosynthetic Paulinella chromatophora FK01 and the phagotrophic Paulinella ovalis using amplified DNA from single (or a few) cells. A parallel objective is to sequence the chromatophore genome from Paulinella chromatophora FK01 to determine the magnitude of endosymbiotic gene transfer (EGT) versus gene loss driving the process of organelle genome reduction. Paulinella ovalis genome sequencing will be critical for comparative "before−after endosymbiosis" analyses to untangle the impact of the endosymbiont gene complement to host nuclear genome evolution. Genome−level comparative analyses will reveal the genetic and biochemical evolutionary inventions that allowed the transition from heterotrophy to photoautotrophy.